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Methamphetamine use and Methicillin-resistant Staphylococcus aureus skin infections.

Methicillin-resistant Staphylococcus aureus methicillin-resistant Staphylococcus aureus Methicillin-aminoglycoside resistant Staphylococcus aureus, MRSA An organism with multiple antibiotic resistances–eg, aminoglycosides, chloramphenicol, clindamycin, erythromycin, rifampin, tetracycline,  (MRSA MRSA Methicillin-resistant Staphylococcus aureus. See MARSA. ) infections and methamphetamine use are emerging public health problems. We conducted a case-control investigation to determine risk factors for MRSA skin and soft tissue infections (SSTIs) in residents of a largely rural southeastern community in the United States United States, officially United States of America, republic (2005 est. pop. 295,734,000), 3,539,227 sq mi (9,166,598 sq km), North America. The United States is the world's third largest country in population and the fourth largest country in area. . Case-patients were persons >12 years old who had culturable SSTIs; controls had no SSTIs. Of 119 SSTIs identified, 81 (68.1%) were caused by MRSA. Methamphetamine use was reported in 9.9% of case-patients and 1.8% of controls. After we adjusted for age, sex, and race, patients with MRSA SSTIs were more likely than controls to have recently used methamphetamine (odds ratio 5.10, 95% confidence interval confidence interval,
n a statistical device used to determine the range within which an acceptable datum would fall. Confidence intervals are usually expressed in percentages, typically 95% or 99%.
 1.55-16.79). MRSA caused most SSTIs in this population. Transmission of MRSA may be occurring among metham.phetamine users in this community.

**********

Methicillin-resistant Staphylococcus aureus (MRSA) is a growing public health problem for urban and rural communities in the United States (1,2). Skin and soft tissue are the most common sites of MRSA infection, comprising >75% of MRSA disease (3,4). Skin and soft tissue infections (SSTIs), commonly caused by S. aureus The aureus (pl. aurei) was a gold coin of ancient Rome valued at 25 silver denarii. The aureus was regularly issued from the 1st century BC to the beginning of the 4th century AD, when it was replaced by the solidus. , annually account for an estimated 11.6 million visits to hospital outpatient departments and emergency departments in the United States (5), and the percentage of SSTIs caused by MRSA in urban emergency departments increased from 29% in 2001 and 2002 to 64% in 2003 and 2004 (6). Some of the first reports of MRSA were in injection drug users in urban Detroit during the early 1980s (7,8).

Illegal methamphetamine use in the United States led to a rising number of methamphetamine-related hospital admissions from the early 1980s through the early 2000s (9). In 2004, 0.2% of the national population [greater than or equal to] 12 years of age reported using methamphetamine in the previous month; 0.6% reported using it in the previous year (10). The prevalence of methamphetamine use has been reported to be >5% in at-risk populations such as young men from low-income, urban neighborhoods (11) and urban HIVpositive men who have sex with men Men who have sex with men (MSM) is a term used mostly in the United States to classify men who engage in sex with other men, regardless of whether they self-identify as gay, bisexual, or heterosexual.  (12).

On August 2, 2005, the Georgia Division of Public Health invited the Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center.  (CDC See Control Data, century date change and Back Orifice.

CDC - Control Data Corporation
) to assist in an on-site investigation of increased SSTIs among patients of a low-cost, fee-for-service clinic in rural Georgia. The clinic's nurse practitioner nurse practitioner
n. Abbr. NP
A registered nurse with special training for providing primary health care, including many tasks customarily performed by a physician.
 had noted a history of methamphetamine use in multiple patients with SSTIs. Methamphetamine use has been associated with MRSA skin infections among urban HIV-positive men who have sex with men (12), but no study has evaluated the association of methamphetamine use and MRSA infection in a community with a large rural population. The objectives of this investigation were to define the public health effects and to determine risk factors, including methamphetamine use, for MRSA SSTI SSTI State Science & Technology Institute (Westerville, OH)
SSTI Skin and Soft Tissue Infection
SSTI Small Spacecraft Technology Initiative
SSTI Skin and Skin Structure Infection
SSTI Six Sigma Technical Institute
 among residents of a community in the southeastern United States.

Methods

Epidemiologic Investigation

We conducted a prospectively enrolled case-control investigation at 3 emergency departments and 3 urgent care clinics in Georgia from September 6 through October 31, 2005. Two low-cost urgent care clinics that serve primarily low-income populations and all emergency departments in a 3-county area were included in an attempt to capture sites where methamphetamine users might seek medical care for SSTI. The third urgent care clinic was affiliated with one of the participating hospitals but was located in a neighboring county. According to according to
prep.
1. As stated or indicated by; on the authority of: according to historians.

2. In keeping with: according to instructions.

3.
 the 2000 US Census, 43.9% of the population of these 3 counties lives in rural areas (13).

We defined a case-patient as a person > 12 years of age with a laboratory culture-confirmed SSTI who came to a participating emergency department or clinic for treatment during the investigation period. Clinicians at participating institutions identified patients with culturable SSTIs and were asked to incise in·cise
v.
To cut into with a sharp instrument.
, drain, and culture all infected skin and soft tissue. Patients with SSTIs that were not culturable, such as simple cellulitis Cellulitis Definition

Cellulitis is a spreading bacterial infection just below the skin surface. It is most commonly caused by Streptococcus pyogenes or Staphylococcus aureus.
, were not included. Patients whose primary language was not English were enrolled if they could speak English fluently enough to answer survey questions. Patients with new or recurrent SSTI could also be enrolled; however, we excluded patients who had previously enrolled in the investigation.

Controls were patients >12 years of age with no current skin infection who were frequency matched by investigation site at a rate of 3 controls to 1 case-patient with MRSA infection. Controls were excluded if they reported a current skin infection or if infection was identified on physical examination. Persons could be enrolled as control patients if illness was minor and comparable in severity to an SST SST: see airplane. 1. For example, patients with major trauma and critically ill patients were excluded from control selection.

Upon seeking treatment, patients voluntarily consented to be interviewed by trained staff of the participating healthcare facilities, local public health departments, or CDC to identify SSTI case-patients. To ensure as much privacy as possible, the interviews were usually conducted in the patient's room with no family or friends present. The interview survey contained questions about demographics, clinical history, and potential risk factors for SSTI. Each patient was asked a specific question about methamphetamine use: "In the past 3 months, have you used methamphetamine (crystal meth meth
n.
Methamphetamine hydrochloride.
 or meth)?" If the patient answered yes, 2 follow-up questions were asked: 1) "How did you take methamphetamine?" with the choices "smoked or inhaled," "injected," or "swallowed or took pills," and 2) "Have you shared drug equipment or rinse water with anyone else, including a significant other?" To identify healthcare exposure, patients were asked whether they had had surgery or dialysis or if they had stayed overnight in a hospital within the previous 3 months. All patients, and their parents if the patients were <18 years of age, were given a letter explaining the investigation and asked to give verbal informed consent to enroll in the investigation.

We examined trends in S. aureus skin infections and cultures at one of the main emergency departments in our investigation by reviewing billing codes and laboratory microbiology reports from January 2004 through September 2005, the start of the case-control survey investigation. This investigation was deemed exempt from review by the CDC Institutional Review Board because it was part of a public health response by CDC and the Georgia Division of Public Health.

Laboratory Investigation

Specimens were obtained from at least 1 infection site in all case-patients. Staff at all 3 hospital emergency departments and the urgent care clinic affiliated with 1 of the hospitals collected cultures and performed antimicrobial drug susceptibility testing at their facility. Two low-cost, urgent care clinics sent all cultures to CDC for culture and antimicrobial drug susceptibility testing. All 6 investigation sites sent both MRSA and methicillin-susceptible S. aureus (MSSA MSSA Methicillin-Sensitive Staphylococcus Aureus
MSSA Microscopy Society of Southern Africa
MSSA Maryland Saltwater Sportfishermen's Association
MSSA Military Selective Service Act
MSSA Mid-South Sociological Association
MSSA Minnesota Social Service Association
) isolates to CDC for further characterization.

All available isolates from methamphetamine users and a random sample of isolates not related to methamphetamine use from each of the 6 investigation sites were tested at CDC for antimicrobial susceptibility by the Clinical and Laboratory Standards Institute broth microdilution method (14). We tested for susceptibility to chloramphenicol chloramphenicol (klōr'ămfĕn`əkŏl'), antibiotic effective against a wide range of gram-negative and gram-positive bacteria (see Gram's stain). It was originally isolated from a species of Streptomyces bacteria. , clindamycin, daptomycin, doxycycline doxycycline /doxy·cy·cline/ (dok?se-si´klen) a semisynthetic broad-spectrum tetracycline antibiotic, active against a wide range of gram-positive and gram-negative organisms; used also as d. calcium and d. hyclate. , erythromycin erythromycin (ĭrĭth'rōmī`sĭn), any of several related antibiotic drugs produced by bacteria of the genus Streptomyces (see antibiotic). , gentamicin gentamicin /gen·ta·mi·cin/ (jen?tah-mi´sin) an aminoglycoside antibiotic complex isolated from bacteria of the genus Micromonospora, , levofloxacin, linezolid, oxacillin oxacillin /ox·a·cil·lin/ (ok?sah-sil´in) a semisynthetic penicillinase-resistant penicillin used as the sodium salt in infections due to penicillin-resistant, gram-positive organisms. , penicillin, rifampin rifampin (rĭfăm`pĭn), antibiotic used in the treatment of tuberculosis. It is also used to eliminate the meningococcus microorganism from carriers and to treat leprosy, or Hansen's disease. , tetracycline tetracycline (tĕ'trəsī`klēn), any of a group of antibiotics produced by bacteria of the genus Streptomyces. They are effective against a wide range of Gram positive and Gram negative bacteria, interfering with protein , trimethoprim-sulfamethoxazole, and vancomycin vancomycin (văn'kōmī`sĭn), antibiotic resembling penicillin in the way it acts. It is derived from the bacterium Streptomyces orientalis, which was isolated from soil of India and Indonesia. . In addition, we performed the cefoxitin disk diffusion test to predict mecA-mediated resistance to oxacillin (14) and the D-zone test for inducible clindamycin resistance (15). Isolates were also tested by using PCR PCR polymerase chain reaction.

PCR
abbr.
polymerase chain reaction


Polymerase chain reaction (PCR) 
 for genes encoding the staphylococcal staphylococcal

pertaining to Staphylococcus spp.


staphylococcal clumping test
used as a means of measuring the quantity of fibrinogen-split products in a sample of blood.
 cassette chromosome mec (SCCmec) resistance complex, Panton-Valentine leukocidin Panton-Valentine leukocidin

a nonhemolytic toxin produced by Staphylococcus aureus which kills segmented neutrophils and macrophages.
 (PVL PVL Periventricular Leukomalacia
PVL Prevail
PVL Parameter Value Language
PVL Pade Via Lanczos (circuit modeling)
PVL Physical Volume Library
PVL Pascack Valley Line (New Jersey Transit commuter rail line) 
) cytotoxin cytotoxin /cy·to·tox·in/ (si´to-tok?sin) a toxin or antibody having a specific toxic action upon cells of special organs.

cy·to·tox·in
n.
, and toxic shock syndrome toxic shock syndrome (TSS). acute, sometimes fatal, disease characterized by high fever, nausea, diarrhea, lethargy, blotchy rash, and sudden drop in blood pressure. It is caused by Staphylococcus aureus, an exotoxin-producing bacteria (see toxin).  toxin (16). Chromosomal DNA DNA: see nucleic acid.
DNA
 or deoxyribonucleic acid

One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes.
 was analyzed by pulsed-field gel electrophoresis gel electrophoresis
n.
Electrophoresis performed in a gel composed of agarose, polyacrylamide, or starch.
 (PFGE PFGE Pulsed-Field Gel Electrophoresis ) after digestion with SmaI restriction endonuclease restriction endonuclease

one of over 200 enzymes isolated from bacteria that cleave any DNA molecule at specific sites which are usually palindromes of 4 to 10 or so nucleotides to yield a collection of restriction DNA fragments that can be separated, usually by electrophoresis in
 (17). The relatedness of PFGE patterns in different isolates was defined by using Dice coefficients and 80% relatedness by the unweighted pair-group method with arithmetic averages (Applied Maths, BioNumerics, Austin, TX, USA) (18).

Statistical Methods

We conducted univariate analysis of the data to describe patient demographics and compared binary and If two conditions are combined by and, they must both be true for the compound condition to be true as well.

Likewise, two bits may be combined with and:

x y x AND y
0 0 0
0 1 0
1 0 0
1 1 1

I.e.
 categorical variables with the [x.sup.2] test; continuous variables were compared by using the t test with unequal variances. We evaluated risk factors for MRSA SSTIs by using conditional logistic regression In statistics, logistic regression is a regression model for binomially distributed response/dependent variables. It is useful for modeling the probability of an event occurring as a function of other factors.  with stratification by investigation site. Risk estimates were adjusted for age (categorized as [less than or equal to]18 years, 19-34 years, 35-64 years, and [greater than or equal to]65 years), sex, and race (categorized as white and nonwhite non·white  
n.
A person who is not white.



nonwhite adj.
) because they were potential confounding variables.

Results

Epidemiologic Investigation

We identified 119 case-patients with skin infections in the investigation. MRSA was isolated from 81 (68.1%) of the skin and soft tissue cultures, MS SA from 20 (16.8%), and bacteria other than S. aureus from 18 (15.1%) (Table 1). Compared with controls with no skin infection, a higher percentage of patients with MRSA SSTIs were male (p<0.001). The proportion of patients that were male did not differ significantly between controls and patients with either MSSA or non--S. aureus SSTIs (p = 0.67 for MSSA, p = 0.12 for non--S. aureus) or between patients with MRSA and MSSA SSTIs (p = 0.16).

Fifteen patients who reported recently using methamphetamine were identified: 8 with MRSA SSTIs, 2 with MSSA SSTIs, and 5 controls. Half (8 [53.3%]) of the methamphetamine users were male. Ten percent of patients with MRSA skin infections (8/81) reported using methamphetamine in the past 3 months, significantly more than the 2% of controls (5/283) who reported this behavior (p<0.001). After adjusting for age, sex, and race, we determined that patients with MRSA SSTI were significantly more likely to have recently used methamphetamine than were controls (adjusted odds ratio [AOR AOR

The ISO 4217 currency code for Angolan Reajustado Kwanza.
] 5.10, 95% confidence interval [CI] 1.55-16.79) (Table 2). Of the 8 methamphetamine users with MRSA SSTIs, most (5 [62.5%]) smoked or inhaled the drug. Only 1 (12.5%) injected the drug, and 1 (12.5%) took the drug orally. For 1 methamphetamine user with MRSA SSTI, we could not determine the route of drug administration. Of the 8 methamphetamine users with MRSA SSTIs in our investigation, 2 (25.0%) reported sharing drug equipment or rinse water with other persons; we did not have information on drug-sharing behavior for 1 methamphetamine user with a MRSA SSTI.

In our study population, having had a skin infection within the previous 3 months was the factor most strongly associated with current MRSA skin infection (AOR 7.92, 95% CI 4.10-15.28) (Table 2). Recent sexual contact with someone with a skin infection was also a significant risk factor for MRSA skin disease (AOR 5.42, 95% CI 1.6817.50), when compared with recent sexual contact with a person without a skin infection. Frequent skin-picking behavior was independently associated with MRSA SSTI (AOR 2.53, 95% CI 1.22-5.23). Crowded living conditions living conditions nplcondiciones fpl de vida

living conditions nplconditions fpl de vie

living conditions living
, defined as >1 person per bedroom, had a small but significant association with MRSA SSTI (AOR 1.78, 95% CI 1.004-3.15).

Only 10% of MRSA case-patients had healthcare-associated risk factors traditionally associated with MRSA infection, namely, recent hospitalization, surgery, or dialysis. Additional factors not significantly associated with MRSA SSTI in our study population included use of antimicrobial agents Antimicrobial agents

Chemical compounds biosynthetically or synthetically produced which either destroy or usefully suppress the growth or metabolism of a variety of microscopic or submicroscopic forms of life.
 in the previous 6 months, recent stays in a jail or prison, bathing less than daily, history of diabetes or liver disease Liver Disease Definition

Liver disease is a general term for any damage that reduces the functioning of the liver.
Description

The liver is a large, solid organ located in the upper right-hand side of the abdomen.
, recent tattoo or body piercing body piercing Body image A disruption of a mucocutaneous surface with jewelry or dangling artifices. See Tattoos. , and participation in contact sports in the previous 3 months. In addition, very few or no patients were HIV HIV (Human Immunodeficiency Virus), either of two closely related retroviruses that invade T-helper lymphocytes and are responsible for AIDS. There are two types of HIV: HIV-1 and HIV-2. HIV-1 is responsible for the vast majority of AIDS in the United States.  positive (2 [0.5%]), homeless (0), or recently had sex with someone of the same sex (7 [1.6%]), suggesting that none of these were significant risk factors for MRSA SSTI in this population.

The number of visits for S. aureus skin infections at one of the main emergency departments in our investigation increased from [approximately equal to] 1 per 1,000 emergency department visits to 12 per 1,000 visits over the 20 months leading up to the investigation (Figure 1). This emergency department accounted for 46.2% of all study participants in our investigation. Over the same period, MRSA infections increased from 2 to 38 per month in the same emergency department. Most emergency department S. aureus cultures for both SSTls and non-SSTIs were resistant to methicillin methicillin /meth·i·cil·lin/ (meth?i-sil´in) a semisynthetic penicillin highly resistant to inactivation by penicillinase; used as the sodium salt.

meth·i·cil·lin
n.
, with the prevalence of methicillin-resistance remaining stable over the same 20-month period (median 82%, range 50-100%).

Laboratory Investigation

MRSA (n = 32) and MSSA (n = 13) isolates tested were commonly susceptible to clindamycin, daptomycin, doxycycline, gentamicin, levofloxacin, linezolid, rifampin, tetracycline, trimethoprim-sulfamethoxazole, and vancomycin (Table 3). None of the MRSA isolates and only 1 (7.7%) of the MSSA isolates had inducible clindamycin resistance. MRSA susceptibility patterns of isolates from methamphetamine users and nonusers were similar, except that both MRSA isolates susceptible to erythromycin were found in those who did not use methamphetamine. The MSSA isolate from a methamphetamine user was susceptible to all but penicillin.

We detected genes for PVL in all MRSA isolates and 5 (41.7%) MSSA isolates; however, the MSSA isolate from a methamphetamine user did not carry the PVL locus. All available MRSA isolates from 6 methamphetamine users and 21 nonusers of methamphetamine had type IV SCCmec resistance complex and were PFGE type USA300. Most of the MRSA isolates were a single strain, PFGE type USA300-0114 (4 [66.7%] were methamphetamine users, 15 [71.4%] were non-methamphetamine users) (Figure 2). One third (33.3%) of MRSA isolates from methamphetamine users and one fifth (19.0%) of MRSA isolates from non-methamphetamine users were variants of USA3000114, such as USA300-0047.

Discussion

MRSA caused over two thirds of all skin infections in the Georgia community we investigated, which is among the highest reported rates of MRSA in SSTI nationwide (16). We found that many previously known risk factors for MRSA skin infection, such as recent skin infection and household contact with someone with a skin infection (19), were common in this population. However, we also identified a novel association between MRSA skin infections and methamphetamine use in a community with a large rural population. Methamphetamine use was reported in nearly 1 in 10 patients with MRSA SSTI and was more common in patients with MRSA skin infections than in patients without skin infections. While most community-associated MRSA SSTI occur in persons without defined risk factors (16), some settings such as prisons and military training facilities appear to facilitate and amplify MRSA transmission (20,21). A similar amplification of transmission may be occurring among methamphetamine users in this community.

Methamphetamine use is associated with a number of socioeconomic and behavioral risk factors that may predispose pre·dis·pose
v.
To make susceptible, as to a disease.
 persons to MRSA SSTI. We found that MRSA SSTI was associated with living with someone with a skin infection, which may increase skin contact with infected persons. Skin-picking was also associated with MRSA SSTI. Methamphetamine use causes formication formication /for·mi·ca·tion/ (for?mi-ka´shun) a sensation as if small insects were crawling on the skin.

for·mi·ca·tion
n.
, a sensation of something crawling on the body or under the skin, which can lead to skin-picking behavior, skin breakdown, and portals of infection. Other poor hygiene habits that can break the skin, such as fingernail fin·ger·nail
n.
The nail on a finger.
 biting, have been associated with MRSA SSTI (12). Methamphetamine use may be associated with limited access to medical care, stays in correctional facilities, and homelessness, all of which have been associated with MRSA SSTI in previous studies (20,22). However, our investigation did not find these to be significant risk factors for MRSA SSTI in this population.

[FIGURE 1 OMITTED]

Methamphetamine use has been associated with HIV (23) and sexually transmitted bacterial infections (24), purportedly from increased unprotected sex Unprotected sex refers to any act of sexual intercourse in which the participants use no form of barrier contraception. Sexually transmitted infections
Specifically, unprotected sex
 related to the sexually stimulating property of the drug. A study among urban HIV-positive men who have sex with men found that, in addition to methamphetamine use, use of other sexually stimulating drugs such as nitrates ("poppers poppers Drug slang A regional street term for amyl nitrate or isobutyl nitrite ") and sildenafil sildenafil /sil·den·a·fil/ (sil-den´ah-fil?) a phosphodiesterase inhibitor that relaxes the smooth muscle of the penis, facilitating blood flow to the corpus cavernosum; used as the citrate salt to treat erectile dysfunction.  (e.g., Viagra) was associated with MRSA SSTI (12). These previous findings and the results of the current investigation suggest that the use of methamphetamine and other sexually stimulating drugs may increase direct skin-to-skin sexual contact and transmission of MRSA, which can be transmitted through sexual contact (25). We found an increased risk for MRSA SSTI in case-patients who had recently had sex with someone with a skin infection.

Injection of the drug may act as a method of introducing the bacteria into the skin if users fail to clean injection sites or share drug paraphernalia drug paraphernalia Controlled paraphernalia Substance abuse As defined in a regulatory context, DP is a hypodermic syringe, needle, metal or plastic (snorting) tube, or other instrument or implement or combination adapted for the administration of controlled  and other potentially contaminated contaminated,
v 1. made radioactive by the addition of small quantities of radioactive material.
2. made contaminated by adding infective or radiographic materials.
3. an infective surface or object.
 items (26). Injection of methamphetamine can lead to transmission of bloodborne pathogens when injection equipment is shared, as demonstrated in an outbreak of hepatitis B Hepatitis B Definition

Hepatitis B is a potentially serious form of liver inflammation due to infection by the hepatitis B virus (HBV). It occurs in both rapidly developing (acute) and long-lasting (chronic) forms, and is one of the most common chronic
 among methamphetamine users in Wyoming (27). A recent case series of 14 patients with MRSA necrotizing fasciitis necrotizing fasciitis
n.
Tissue death such as that associated with group A streptococcus infection.


Necrotizing fasciitis 
 found that 43% of the patients had current or past injection drug use (28). In contrast to early reports of MRSA in urban injection drug users, our investigation suggested that MRSA skin infections in methamphetamine users are not necessarily due to unclean drug injection. Few methamphetamine users in our population injected the drug or shared equipment; rather, the methamphetamine users in this community commonly smoked or inhaled the drug.

The absolute number of SSTIs at 1 emergency department in this investigation increased during the 18 months preceding the investigation, but the percentage of MRSA isolates was stable over that period. This increase in SSTIs led to a concomitant increase in MRSA SSTIs, which were more common among men, and echoes repeated reports of MRSA SSTI outbreaks in male populations (20,29). This sex difference was not due to increased methamphetamine use in men in our population, since our population of surveyed methamphetamine users was evenly divided between the sexes. We also did not find many MRSA infections in nonwhite patients. This finding contrasts with previous reports of higher incidence of MRSA SSTIs in African Americans in urban centers compared to other races (4) and likely reflects the predominantly white racial distribution (98.9%) in these 3 rural southeastern US counties (13).

[FIGURE 2 OMITTED]

The laboratory investigation found that the most common MRSA strain causing community SSTI was PFGE type USA300-0114, a highly conserved strain that has been implicated im·pli·cate  
tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates
1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot.

2.
 in multiple community outbreaks (19). The second most common MRSA strain in this community, and the only other strain found among methamphetamine users, was USA300-0047, which has only a 1-band difference from USA300-0114. MRSA SSTIs in methamphetamine users were not due to a novel or unusual strain of MRSA but rather the most common strain of MRSA in community settings across the United States.

Our investigation is subject to some limitations. First, we did not identify nor do we have data on every SSTI patient who came to the participating clinics and emergency departments for treatment; not every patient with SSTI provided specimens for culture or participated in our survey. Second, we relied on patient report of methamphetamine use and did not conduct drug screens for confirmation. Third, we excluded patients who could only speak Spanish, which may have added to the low number of Hispanic study participants and affected the generalizability of the results. However, Hispanic, foreign-born, and non-English primary speakers each comprise only 5%-10% of the population of these 3 counties (13). Fourth, we were unable to test for other physiologic theories of why methamphetamine may be associated with MRSA, which include weakening the immune system immune system

Cells, cell products, organs, and structures of the body involved in the detection and destruction of foreign invaders, such as bacteria, viruses, and cancer cells. Immunity is based on the system's ability to launch a defense against such invaders.
 and predisposing users to MRSA carriage by changing the nasal environment. Fifth, we were unable to test whether methamphetamine itself or drug paraphernalia were contaminated with MRSA. Lastly, transmission of MRSA in this population may have occurred in either the community or in the healthcare setting; for some cases, we were unable to determine the origin of the community strains.

Our investigation has direct implications for clinicians. Most clinicians in the participating emergency departments and urgent care clinics did not routinely drain or culture SSTIs. Incision and drainage Incision and drainage is a minor surgical procedure to release pus or pressure built up under the skin, such as from an abscess or boil. It is performed by treating the area with an antiseptic, such as iodine based solution, and then making a small incision to puncture the skin  is a primary therapy for SSTI, and empiric antimicrobial drug therapy may be given in addition to incision and drainage (30). Because of the growing and changing resistance patterns in the community, clinicians should consider culturing SSTI (30). In this population, antimicrobial agents currently recommended for treatment of MRSA (e.g., clindamycin, doxycycline, and trimethoprim-sulfamethoxazole) would be appropriate choices for empiric treatment of outpatient SSTI because of low prevalence of resistance (30.) Patients should also be educated about the risks for transmission through household and sexual skin-to-skin contact. Transmission of MRSA in this community is likely due to various factors, and some of these community strains may have been transmitted through healthcare exposure.

Patients with MRSA SSTIs who seek treatment may help clinicians identify a vulnerable population of methamphetamine users. Prevention measures, such as improved hygiene and correct care for wounds, may be helpful when directed at methamphetamine users. However, MRSA SSTIs in methamphetamine users may also impact family and community members who do not use methamphetamine. The same strains of MRSA were circulating among both users and nonusers in our investigation. Public health officials and clinicians should be aware of proper identification, appropriate treatment, prevention of MRSA SSTIs, and the link between methamphetamine use and these SSTIs.

Acknowledgments

We thank our collaborators at all the participating hospitals and clinics, the Northwest Georgia Northwest Georgia includes the counties of:
  • Dade County
  • Walker County
  • Catoosa County
  • Whitfield County
  • Murray County
  • Gordon County
  • Chattooga County
  • Floyd County
  • Bartow County
  • Paulding County
  • Polk County
  • Haralson County
 Health District, the Georgia Division of Public Health, and CDC. We also thank Stanley H. Cohen cohen
 or kohen

(Hebrew: “priest”) Jewish priest descended from Zadok (a descendant of Aaron), priest at the First Temple of Jerusalem. The biblical priesthood was hereditary and male.
 for his support and thoughtful discussion of statistical analysis, and Connie Hogle for her editorial comments.

Dr Cohen is a medical epidemiologist in the Respiratory Diseases Branch of the Division of Bacterial Diseases bacterial diseases

Diseases caused by bacteria. The most common infectious diseases, they range from minor skin infections to bubonic plague and tuberculosis. Until the mid-20th century, bacterial pneumonia was probably the leading cause of death among the elderly.
 at CDC. This investigation was completed when he was an Epidemic Intelligence Service The Epidemic Intelligence Service is a program of the United States' Centers for Disease Control and Prevention. Established in 1951 due to biological warfare concerns arising from the Korean War, it has become a hands-on two-year postgraduate training program in epidemiology, with  Officer in the Division of Healthcare Quality Promotion. His primary research interests are the epidemiology of antimicrobial-resistant bacteria, pediatric patient pediatric patient Child, see there  and drug safety, and vaccine-preventable diseases.

References

(1.) Stevenson KB, Searle K, Stoddard G J, Samore M. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci enterococci

bacteria in the genus Enterococcus.
 in rural communities, western United States Noun 1. western United States - the region of the United States lying to the west of the Mississippi River
West

Santa Fe Trail - a trail that extends from Missouri to New Mexico; an important route for settlers moving west in the 19th century
. Emerg Infect Dis. 2005; 11:895-903.

(2.) Groom AV, Wolsey DH, Naimi TS, Smith K, Johnson S, Boxrud D, et al. Community-acquired methicillin-resistant Staphylococcus aureus in a rural American Indian American Indian
 or Native American or Amerindian or indigenous American

Any member of the various aboriginal peoples of the Western Hemisphere, with the exception of the Eskimos (Inuit) and the Aleuts.
 community. JAMA JAMA
abbr.
Journal of the American Medical Association
. 2001;286:1201-5.

(3.) Naimi TS, LeDell KH, Boxrud DJ, Groom AV, Steward CD, Johnson SK, et al. Epidemiology and clonality of community-acquired methicillin-resistant Staphylococcus aureus in Minnesota, 1996-1998. Clin Infect Dis. 2001 ;33:990-6.

(4.) Fridkin SK, Hageman JC, Morrison M, Sanza LT, Como-Sabetti K, Jernigan JA, et al. Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med. 2005;352:1436-44.

(5.) McCaig LF, McDonald LC, Mandal S, Jernigan DB. Staphylococcus staphylococcus (stăf'ələkŏk`əs), any of the pathogenic bacteria, parasitic to humans, that belong to the genus Staphylococcus. The spherical bacterial cells (cocci) typically occur in irregular clusters [Gr.  aureus-associated skin and soft tissue infections in ambulatory care ambulatory care
n.
Medical care provided to outpatients.


ambulatory care,
n the health services provided on an outpatient basis to those who can visit a health care facility and return home the same day.
. Emerg Infect Dis. 2006;12:1715-23.

(6.) Moran G J, Amii RN, Abrahamian FM, Talan DA. Methicillin-resistant Staphylococcus aureus in community-acquired skin infections. Emerg Infect Dis. 2005; 11:928-30.

(7.) Levine DP, Cushing RD, Jui J, Brown WJ. Community-acquired methicillin-resistant Staphylococcus' aureus endocarditis endocarditis (ĕn'dōkärdī`tĭs), bacterial or fungal infection of the endocardium (inner lining of the heart) that can be either acute or subacute.  in the Detroit Medical Center The Detroit Medical Center is a Detroit-based non-profit corporation that owns and operates nine general and specialty hospitals in southeast Michigan. Detroit Medical Center hospitals include:
. Ann Intern Med. 1982;97:330-8.

(8.) Saravolatz LD, Markowitz N, Arking L, Pohlod D, Fisher E. Methicillin-resistant Staphylococcus aureus. Epidemiologic observations during a community-acquired outbreak. Ann Intern Med. 1982;96:11-6.

(9.) Cunningham JK, Liu LM. Impacts of federal ephedrine ephedrine (ĭfĕd`rĭn, ĕf`ĭdrēn'), drug derived from plants of the genus Ephedra (see Pinophyta), most commonly used to prevent mild or moderate attacks of bronchial asthma.  and pseudoephedrine pseudoephedrine /pseu·do·ephed·rine/ (-e-fed´rin) one of the optical isomers of ephedrine; used as the hydrochloride or sulfate salt as a nasal decongestant.

pseu·do·e·phed·rine
n.
 regulations on methamphetamine-related hospital admissions. Addiction. 2003;98:1229-37.

(10.) Substance Abuse and Mental Health Services Administration The Substance Abuse and Mental Health Services Administration (SAMHSA), an operating division of the Health and Human Services Department (HHS), was established in 1992 by the Alcohol, Drug Abuse, and Mental Health Administration Reorganization Act (Pub. L. No. 102-321). . Results from the 2004 National survey on drug use and health: national findings, 2005 [cited 2007 Sep 7]. Available from http://www.oas.samhsa.gov/nsduh/2k4nsduh/2k4results/2k4results.htm

(11.) Centers for Disease Control and Prevention. Methamphetamine use and HIV risk behaviors among heterosexual men--preliminary results from five northern California Northern California, sometimes referred to as NorCal, is the northern portion of the U.S. state of California. The region contains the San Francisco Bay Area, the state capital, Sacramento; as well as the substantial natural beauty of the redwood forests, the northern  counties, December 2001-November 2003. MMWR MMWR Morbidity & Mortality Weekly Report Epidemiology A news bulletin published by the CDC, which provides epidemiologic data–eg, statistics on the incidence of AIDS, rabies, rubella, STDs and other communicable diseases, causes of mortality–eg,  Morb Mortal Wkly Rep. 2006;55:273-7.

(12.) Lee NE, Taylor MM, Bancroft E, Ruane PJ, Morgan M, McCoy L, et al. Risk factors for community-associated methicillin-resistant Staphylococcus" aureus skin infections among HIV-positive men who have sex with men. Clin Infect Dis. 2005;40:1529-34.

(13.) US Census Bureau Noun 1. Census Bureau - the bureau of the Commerce Department responsible for taking the census; provides demographic information and analyses about the population of the United States
Bureau of the Census
. US Census Bureau American FactFinder, 2000 [cited 2007 Sep 7]. Available from http://www.factfinder.census.gov/home/saff/main.html?_lang+en

(14.) Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. Sixteenth informational supplement. CLSI CLSI Clinical and Laboratory Standards Institute (Wayne, PA)
CLSI Cisco Link Services Interface
 document M 100-S16. Wayne (PA): The Institute; 2006.

(15.) Jorgensen JH, Crawford SA, McElmeel ML, Fiebelkorn KR. Detection of inducible clindamycin resistance of staphylococci staph·y·lo·coc·cus  
n. pl. staph·y·lo·coc·ci
A spherical gram-positive parasitic bacterium of the genus Staphylococcus, usually occurring in grapelike clusters and causing boils, septicemia, and other infections.
 in conjunction with performance of automated broth susceptibility testing. J Clin Microbiol. 2004;42:1800-2.

(16.) Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB, et al. Methicillin-resistant Staphylococcus aureus infections among emergency department patients in 11 U.S. cities. N Engl J Med. 2006;355:666-74.

(17.) Maslow J, Slutsky A, Arbeit R. Application of pulsed-field gel electrophoresis to molecular epidemiology molecular epidemiology Molecular medicine An evolving field that combines the tools of standard epidemiology–case studies, questionnaires and monitoring of exposure to external factors with the tools of molecular biology–eg, restriction endonucleases, . In: Persing D, Smith T, Tenover F, White T, editors. Diagnostic molecular microbiology: principles and applications. Washington: American Society for Microbiology The American Society for Microbiology (ASM) is a scientific organization, based in the United States although with over 43,000 members throughout the world. It is the largest single life science professional organization and its members include those whose interests encompass basic ; 1993. p. 563-72.

(18.) McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, Tenover FC. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus Staphylococcus au·re·us
n.
A bacterium that causes furunculosis, pyemia, osteomyelitis, suppuration of wounds, and food poisoning.


Staphylococcus aureus Staphylococcus pyogenes
 isolates from the United States: establishing a national database. J Clin Microbiol. 2003;41:5113-20.

(19.) Kazakova SV, Hageman JC, Matava M, Srinivasan A, Phelan L, Garfinkel B, et al. A clone of methicillin-resistant Staphylococcus aureus among professional football players. N Engl J Med. 2005;352:468-75.

(20.) Centers for Disease Control and Prevention. Methicillin-resistant Staphylococcus aureus infections in correctional facilities-Georgia, California, and Texas, 2001-2003. MMWR Morb Mortal Wkly Rep. 2003;52:992-6.

(21.) Campbell KM, Vaughn AF, Russell KL, Smith B, Jimenez DL, Barrozo CP, et al. Risk factors for community-associated methicillin-resistant Staphylococcus aureus infections in an outbreak of disease among military trainees in San Diego, California “San Diego” redirects here. For other uses, see San Diego (disambiguation).
San Diego is a coastal Southern California city located in the southwestern corner of the continental United States. As of 2006, the city has a population of 1,256,951.
, in 2002. J Clin Microbiol. 2004;42:4050-3.

(22.) Young DM, Harris HW, Charlebois ED, Chambers H, Campbell A, Perdreau-Remington F, et al. An epidemic of methicillin-resistant Staphylococcus aureus soft tissue infections among medically underserved patients. Arch Surg. 2004; 139:947-51.

(23.) Molitor F, Truax SR, Ruiz JD, Sun RK. Association of methamphetamine use during sex with risky sexual behaviors and HIV infection among non-injection drug users. West J Med. 1998;168:93-7.

(24.) Hirshfield S, Remien RH, Walavalkar I, Chiasson MA. Crystal methamphetamine use predicts incident STD (Subscriber Trunk Dialing) Long distance dialing outside of the U.S. that does not require operator intervention. STD prefix codes are required and billing is based on call units, which are a fixed amount of money in the currency of that country.  infection among men who have sex with men recruited online: a nested case-control study A nested case-control study is a type of study design where new case controls are applied into cohorts which were defined before the study begins.

Compared with case-control study, nested case-control study can reduce 'recall bias' and temporal ambiguity, and compared with
. J Med Internet Res. 2004;6:e41.

(25.) Cook HA, Furuya EY, Larson E, Vasquez G, Lowy FD. Heterosexual transmission of community-associated methicillin-resistant Staphylococcus aureus. Clin Infect Dis. 2007;44:410-3.

(26.) Gordon R J, Lowy FD. Bacterial infections in drug users. N Engl J Med. 2005;353:1945-54.

(27.) Vogt TM, Perz JF, Van Houten CK Jr, Harrington R, Hansuld T, Bialek SR, et al. An outbreak of hepatitis B virus infection among methamphetamine injectors: the role of sharing injection drug equipment. Addiction. 2006; 101:726-30.

(28.) Miller LG, Perdreau-Remington F, Rieg G, Mehdi S, Perlroth J, Bayer AS, et al. Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med. 2005;352:1445-53.

(29.) Centers for Disease Control and Prevention. Methicillin-resistant Staphylococcus aureus infections among competitive sports participants Colorado, Indiana, Pennsylvania, and Los Angeles County, 2000-2003. MMWR Morb Mortal Wkly Rep. 2003;52:793-5.

(30.) Gorwitz R J, Jernigan DB, Powers JH, Jernigan JA; Participants in the Centers for Disease Control and Prevention-Convened Experts' Meeting on Management of MRSA in the Community. Strategies for clinical management of MRSA in the community: summary of an experts' meeting convened by the Centers for Disease Control and Prevention, 2006 [cited 2007 Sep 7]. Available from http://www.cdc.gov/ncidod/dhqp/pdf/ar/CAMRSA_ExpMtgStrategies.pdf

Address for correspondence: Adam L. Cohen, Respiratory Diseases Branch, Division of Bacterial Diseases, Centers for Disease Control and Prevention, 1600 Clifton Rd NE, Mailstop C23, Atlanta, GA 30333, USA; email: alcohen1@cdc.gov

Adam L. Cohen, * Carrie Shuler, * ([dagger]) Sigrid McAllister, * Gregory E. Fosheim, * Michael G. Brown, ([double dagger]) Debra Abercrombie, ([section]) Karen Anderson, * Linda K. McDougal, * Cherie Drenzek, ([dagger]) Katie Arnold, ([dagger]) Daniel Jernigan, * and Rachel Gorwitz *

* Centers for Disease Control and Prevention, Atlanta, Georgia, USA; ([dagger]) Georgia Division of Public Health, Atlanta, Georgia, USA; ([double dagger]) Kennestone Hospital, Marietta, Georgia, USA; and ([section])Northwest Georgia Health District 1-1, Rome, Georgia, USA
Table 1. Demographic characteristics of study participants with
(case-patients) and without (controls) skin and soft tissue
infections (SSTIs) *

                                    Patients with SSTIs

Characteristic         MRSA (N = 81), no. (%)   MSSA (N = 20), no. (%)

Age, y
  [less than or
    equal to] 18       12 (14.8)                0
  19-34                30 (37.0)                13 (66.0)
  35-64                35 (43.2)                6 (30.0)
  [greater than or
    equal to] 65       4 (4.9)                  1 (5.0)
Male sex
  ([double dagger])    48 (59.3) ([section])    8 (40.0)
Race ([paragraph])
  White                73 (90.1)                18 (90.0)
  Black                5 (6.2)                  2 (10.0)
  Other                3 (3.7)                  0
Hispanic
  ethnicity (#)        2 (2.5)                  0

                       Patients with SSTIs

                       Other ([dagger])         Patients without SSTIs
Characteristic         (N = 18), no. (%)        (N = 284), no. (%)

Age, y
  [less than or
    equal to] 18       2 (11.1)                 18 (6.3)
  19-34                8 (44.4)                 102 (35.9)
  35-64                7 (38.9)                 135 (47.5)
  [greater than or
    equal to] 65       1 (5.6)                  29 (10.2)
Male sex
  ([double dagger])    10 (55.6)                104 (36.6)
Race ([paragraph])
  White                16 (88.9)                244 (85.9)
  Black                2 (11.1)                 36 (12.7)
  Other                0                        3 (1.1)
Hispanic
  ethnicity (#)        0                        4 (1.4)

* MRSA, methicillin-resistant Staphylococcus aureus; MSSA,
methicillin-susceptible S. aureus.

([dagger]) Bacteria other than S. aureus isolated from SSTI in our
investigation included other Staphylococcus spp., viridans group
streptococci, Group B Streptococcus, Enterobacter cloacae,
Stenotrophomonas maltophilia, and mixed flora.

([double dagger]) 6 records did not indicate sex (1 MRSA case, 1 MSSA
case, and 4 controls).

([section]) p < 0.0001, when compared with controls.

([paragraph]) For 1 control, race was not indicated.

(#) 3 records did not indicate ethnicity (2 MRSA cases, 1 other skin
infection).

Table 2. Risk factors for MRSA skin and soft tissue infection *

                                           Case-patients,   Controls,
Risk factors                                  no. (%)        no. (%)

Drug use and medical history
  Recent skin infection                      34 (42.0)       22 (7.8)
  ([double dagger])
  Recent methamphetamine use                  8 (9.9)        5 (1.8)
  (double dagger])
  Antimicrobial agents within 6 months       40 (49.4)      114 (40.1)
  Recent hospitalization, surgery, or         8 (9.9)        27 (9.5)
  dialysis ([double dagger])
  Diabetes                                   10 (12.4)       23 (8.1)
  Liver disease                               1 (1.2)        9 (3.2)
Contact exposure
  Household contact with someone with        21 (25.9)       27 (9.5)
  skin
  infection
  Crowding (>1 person/bedroom)               44 (54.3)      111 (39.1)
  Recent sexual contact                      48 (59.3)      182 (64.1)
  ([double dagger])
  Recent sexual contact with someone          7 (8.6)        6 (2.1)
  with skin infection ([double dagger])
  Recent contact sports                       9 (11.1)       11 (3.9)
  ([double dagger])
  Recent jail ([double dagger])               4 (4.9)        9 (3.2)
Hygiene practices
  Frequent skin picking                      17 (20.1)       24 (8.5)
  Bathe less than daily                       5 (6.2)       31 (10.9)

Risk factors                                  Crude OR (95% CI)

Drug use and medical history
  Recent skin infection                       8.41 (4.54-15.59)
  ([double dagger])
  Recent methamphetamine use                  5.64 (1.80-17.69)
  (double dagger])
  Antimicrobial agents within 6 months        1.43 (0.87-2.34)
  Recent hospitalization, surgery, or         1.06 (0.46-2.44)
  dialysis ([double dagger])
  Diabetes                                    1.61 (0.73-3.57)
  Liver disease                               0.38 (0.05-3.07)
Contact exposure
  Household contact with someone with         3.26 (1.72-6.17)
  skin
  infection
  Crowding (>1 person/bedroom)                2.06 (1.22-3.45)
  Recent sexual contact                       0.85 (0.51-1.42)
  ([double dagger])
  Recent sexual contact with someone          4.28 (1.40-13.08)
  with skin infection ([double dagger])
  Recent contact sports                       2.92 (1.17-7.31)
  ([double dagger])
  Recent jail ([double dagger])               1.46 (0.44-4.90)
Hygiene practices
  Frequent skin picking                       2.77 (1.40-5.47)
  Bathe less than daily                       0.50 (0.19-1.34)

                                           Adjusted OR ([dagger])
Risk factors                                      (95% CI)

Drug use and medical history
  Recent skin infection                       7.92 (4.10-15.28)
  ([double dagger])
  Recent methamphetamine use                  5.10 (1.55-16.79)
  (double dagger])
  Antimicrobial agents within 6 months        1.52 (0.89-2.60)
  Recent hospitalization, surgery, or         1.24 (0.51-2.97)
  dialysis ([double dagger])
  Diabetes                                    2.03 (0.83-4.98)
  Liver disease                               0.59 (0.70-4.91)
Contact exposure
  Household contact with someone with         3.19 (1.58-6.48)
  skin
  infection
  Crowding (>1 person/bedroom)                1.78 (1.004-3.15)
                                                 ([section])
  Recent sexual contact                       0.68 (0.38-1.22)
  ([double dagger])
  Recent sexual contact with someone          5.42 (1.68-17.50)
  with skin infection ([double dagger])
  Recent contact sports                       1.37 (0.47-4.03)
  ([double dagger])
  Recent jail ([double dagger])               1.75 (0.48-6.42)
Hygiene practices
  Frequent skin picking                       2.53 (1.22-5.23)
  Bathe less than daily                       0.56 (0.19-1.67)

* MRSA, methicillin-resistant Staphylococcus aureus, OR, odds ratio;
CI, confidence interval.

([dagger]) All models are adjusted for age, sex, race, and
methamphetamine use, except the model for methamphetamine use, which
is adjusted only for age, sex, and race.

(([double dagger]) Recent = within the 3 months prior to survey.

([section]) p = 0.048.

Table 3. Antimicrobial susceptibility patterns and toxin gene presence
of selected MRSA and MSSA isolates *

Antimicrobial agent or toxin        MRSA isolates       MSSA isolates
                                     ([dagger])       (N = 13), no. (%)
                                  (N = 32), no. (%)

Antimicrobial susceptibility
  Chloramphenicol                    32 (100.0)           10 (76.9)
                                                      ([double dagger])
  Clindamycin                        32 (100.0)           12 (92.3)
    Inducible resistance
     (D-zone test)                        0                1 (7.7)
  Daptomycin                         32 (100.0)          13 (100.0)
  Doxycycline                        32 (100.0)          13 (100.0)
  Erythromycin                         2 (6.5)             6 (46.2)
  Gentamicin                         32 (100.0)          13 (100.0)
  Levofloxacin                        27 (84.4)           12 (92.3)
  Linezolid                          32 (100.0)          13 (100.0)
  Penicillin                              0                2 (15.4)
  Rifampin                           32 (100.0)          13 (100.0)
  Trimethoprim-sulfamethoxazole      32 (100.0)          13 (100.0)
  Vancomycin                         32 (100.0)          13 (100.0)
Toxin gene presence
  Panton-Valentine leukocidin        32 (100.0)            5 (38.5)
  TSST-1                                  0                   0

* MRSA, methicillin-resistant Staphylococcus aureus; MSSA,
methicillin-susceptible Staphylococcus aureus, TSST, toxic shock
syndrome toxin.

([dagger]) Methicillin resistance was determined by the oxacillin
MIC and disk diffusion using a 30-[micro]g cefoxitin disk (14).

([double dagger]) Three (23.1%) isolates had intermediate resistance
to chloramphenicol.
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Author:Cohen, Adam L.; Shuler, Carrie; McAllister,Sigrid; Fosheim, Gregory E.; Brown, Michael G.; Abercromb
Publication:Emerging Infectious Diseases
Date:Nov 1, 2007
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